Prediction by single neurons

ABSTRACT

Associative plasticity rules are described to control the strength of inputs to an artificial neuron. Inputs to a neuron consist of both synaptic inputs and non-synaptic, voltage-regulated inputs. The neuron&#39;s output is voltage. Hebbian and anti-Hebbian-type plasticity rules are implemented to select amongst a spectrum of voltage-regulated inputs, differing in their voltage-dependence and kinetic properties. An anti-Hebbian-type rule selects inputs that predict and counteract deviations in membrane voltage, thereby generating an output that corresponds to a prediction error. A Hebbian-type rule selects inputs that predict and amplify deviations in membrane voltage, thereby contributing to pattern generation. In further embodiments, Hebbian and anti-Hebbian-type plasticity rules are also applied to synaptic inputs. In other embodiments, reward information is incorporated into Hebbian-type plasticity rules. It is envisioned that by following these plasticity rules, single neurons as well as networks may predict and maximize future reward.

CROSS REFERENCE TO RELATED APPLICATIONS

This application is a continuation-in-part of U.S. patent application Ser. No. 12/271,282, Prediction by Single Neurons and Networks, filed Nov. 14, 2008, which claims the benefit of U.S. provisional patent application Ser. No. 60/989,391, Prediction by Single Neurons and Networks, filed Nov. 20, 2007, wherein the entirety of each is incorporated herein by this reference thereto.

BACKGROUND OF THE INVENTION

1. Technical Field

This invention relates generally to the field of neural network models and artificial intelligence. More specifically, this invention relates to a model of the computational function of a single artificial neuron.

2. Description of the Related Art

There has long been an interest in developing artificial systems that exhibit the intelligence of humans or other animals. One means of approaching this challenge has been to create computational systems that incorporate known elements of biological nervous systems. This approach has led to the creation of artificial neural networks. An artificial neural network consists of multiple inter-connected “neurons,” in which the output of each neuron depends on the weighted sum of its inputs. The network as a whole receives external inputs and generates outputs. The goal of the system is to learn to generate appropriate outputs to each input pattern by adjusting the connection weights between neurons. The adjustment of connection weights may occur under the influence of some sort of feedback about the appropriateness of the output.

Neural networks have had some success in generating useful intelligence. But despite the fact that they have been around since the 1950's, significant efforts have failed to result in artificial intelligence that compares to that generated by biological nervous systems. Likewise, the neurons of artificial networks bear only a limited resemblance to biological neurons.

Biological nervous systems have the ability to learn for themselves (i.e. self-organize). A primary goal of research on neural networks has been to create artificial networks that can do the same. Ideally, a network would start with virtually no information about the world but would become knowledgeable over time on its own. Whether or not this could ever be achieved, a practical goal is to develop networks that are as general as possible in what they are able to learn, while having as little information as possible built in from the start.

Neural networks have typically been designed using substantial knowledge of how to solve a specific task. This is most obvious in the case of networks trained under the influence of an externally generated supervisory signal, which essentially tells the network what it is doing wrong. Thus the network is fed expert information. By contrast, biological nervous systems must learn for themselves through trial and error. Likewise, some artificial networks perform unsupervised learning, which by definition does not depend on an external supervisory signal. However, even these networks have generally been designed so that the network learns to perform a particular input-output transformation. Thus the designer builds the network with knowledge of how outputs should depend on inputs. Since the appropriate input-output transformation will be different for different tasks or environments, a network designed for one environment may not be able to adapt to a new environment. By contrast, biology discovers for itself how outputs should depend on inputs, and biological nervous systems can be remarkably adaptable to new environments. The present ideas are based on a computational model of biological neurons.

The goal of a network is to select appropriate outputs, a process that could be referred to as “decision making.” The problem in making decisions is uncertainty about the current and future states of the world. The uncertainty in a prediction is inversely related to the amount of information upon which the prediction is based, and therefore minimizing uncertainty is the same as maximizing information. If the system could accurately predict the state of the world, then the problem would be solved, and the system would merely select the output that it knows is the most advantageous (e.g. the output that maximizes its expected future reward). The process of minimizing uncertainty is thus considered to be formally identical to the process of decision-making, since decisions are rendered trivial in the absence of uncertainty.

Any reference made to “information” herein refers to information that the network or a neuron holds within its biophysical structure. Even a single molecule, such as an ion channel in a neuronal membrane, contains information. By definition, information predicts something. Thus the prediction made by a neuron is entirely conditional on information possessed by the neuron. In the present work, the relevant information is not that which an observer of the network may have about the network or the world.

The present invention can be viewed as an application of fundamental principles of reinforcement learning to the computational function of a single neuron. Reinforcement learning is concerned with how a biological or artificial agent can learn on its own to achieve its goals. Since all of an agent's outputs should be selected in order to promote its future goals, an agent learns to predict “the sum of future rewards.” Although the notion of future rewards is quite abstract and intangible, the agent predicts future reward by predicting concrete stimuli and events that are themselves predictive of future reward. Thus the agent tries to predict the current state of the sensory world because the sensory world is informative about future reward. For example, the sight of food is predictive of the ingestion of food, and thus an agent would like to be able to predict the sight of food.

To learn to make such predictions, the agent relies on prediction errors. A prediction error is the difference between what is expected and what is actually observed. The artificial neuron described here generates a type of prediction error, and uses it to learn to predict an aspect of the world that is itself potentially predictive of future reward. Whereas most past work on reinforcement learning has implemented principles of reinforcement learning at the level of networks and systems, the present work applies these principles to the function of a single neuron, and by extension, to a network of neurons.

Artificial neural networks are composed of multiple interconnected neurons. The output of each neuron is determined by the weighted sum of its inputs. Each input serves as an information source, and in principle, a neuron could have a virtually infinite number of inputs. But a neuron's output depends only on those inputs that have sufficiently high weights. Creating an intelligent network is therefore largely a matter of selecting the appropriate weights. Despite over 50 years of work on this problem, there has not been a generally accepted and universally applicable set of guidelines that specifies the weight that should be given to each of a neuron's inputs. Herein, new principles are described for choosing the weights of a neuron's inputs. Some inputs should be given high weights if they are unpredictable from the neuron's perspective, whereas others should be given high weights if they are effective predictors.

Although there are multiple means by which these new principles might be implemented, perhaps the most attractive embodiment would utilize plasticity algorithms. Real neurons communicate with one another through synapses in which information is traditionally thought to flow in one direction from the pre-synaptic to the post-synaptic neuron. The strength of the connection between two neurons is described by a weight, and many artificial neural networks employ plasticity algorithms that modify the weight according to coincident activity in the pre-synaptic input neuron and the post-synaptic output neuron. A commonly used class of plasticity rules is known as Hebbian. According to a Hebbian rule, a connection weight increases if activity in a pre-synaptic neuron is positively correlated with the activity of a post-synaptic neuron. Thus, if a pre-synaptic neuron excites a post-synaptic neuron at approximately the same time that the post-synaptic neuron is excited, then that connection weight increases. If the pre-synaptic neuron is excited at the same time that the post-synaptic neuron is inhibited, then the connection weight may decline.

A less often used form of plasticity in artificial neural networks is known as “anti-Hebbian.” A Hebbian rule strengthens excitatory or inhibitory inputs that are paired with excitation or inhibition, respectively, and it therefore involves positive feedback. An anti-Hebbian rule does just the opposite and results in negative feedback. Thus an inhibitory input that is active at the same time that the post-synaptic neuron is excited would have its connection weight increased. Anti-Hebbian rules are known to be effective in decorrelating neural activity so as to promote efficient coding, and similarly, in learning to make predictions.

Although both Hebbian and anti-Hebbian rules have been explored in the literature for at least several decades now, the application of these plasticity rules to neural networks has not led to a general solution to the problem of creating artificial intelligence. Although each of these plasticity rules has been shown to have certain virtues, it has not been clear which type of plasticity rule should be applied to a particular neuron or to any of its individual inputs. Herein it is proposed that a particular combination of Hebbian and anti-Hebbian plasticity rules within a single neuron will be useful in creating artificial networks that learn to generate intelligent outputs.

In focusing exclusively on synaptic connectivity between neurons, most work on artificial neural networks has ignored an important aspect of biological neurons. The output of a biological neuron is not determined solely by its synaptic inputs. An approximately equal contribution is made by non-synaptic ion channels. The conductance of many of these ion channels is regulated by membrane voltage. An example would be a voltage-gated potassium channel that opens and inhibits the neuron once the membrane becomes depolarized. There are many different types of voltage-gated potassium channels that can be produced by each neuron, but somehow a particular neuron selectively expresses some types of potassium channels but not others. The rules that govern this selection process in biological neurons are not known, and the neurons of most artificial networks do not possess any analogue of these non-synaptic ion channels. The present invention identifies a key role for non-synaptic ion channels, and utilizes anti-Hebbian plasticity to select amongst different types of non-synaptic ion channel.

SUMMARY OF THE INVENTION

The present invention describes a method of information processing inspired by processes that may occur in biological neurons. The central challenge for a nervous system is to predict “future reward,” since all of the system's “decisions” should be made in order to maximize future reward. The invention specifies rules by which an artificial neuron could learn to make predictions about aspects of the world that are relevant to future reward.

In the preferred embodiment, the output of the neuron is voltage, and the inputs are ionic conductances. Ionic conductances can be depolarizing or hyperpolarizing, and include both neurotransmitter-regulated, synaptic ion channels and voltage-regulated, non-synaptic ion channels. The neuron can receive a large number synaptic inputs from other neurons, and it can express a large number of distinct voltage-regulated ion channels that differ in their voltage-dependence and kinetic properties. Associative plasticity rules are used to select a subset of the most informative inputs from amongst this spectrum of potential inputs.

Whereas a substantial amount of prior art has been devoted to the topic of associative plasticity at synapses, i.e. connection between neurons, the present invention applies associative plasticity rules to voltage-dependent ion channels as well as synapses. Each synapse represents a distinct point in space, but synapses do not differ from one another substantially in their kinetic properties. By contrast, voltage-regulated ion channels vary greatly in their kinetic properties from one channel subtype to another. Thus different channel subtypes carry information from different periods of the past. For example, a channel with fast kinetics carries information only about the very recent past, whereas a channel with slow kinetics carries information derived by averaging across a long period of the past. Associative plasticity enables the neuron to select those ion channel subtypes, and the corresponding periods of the past, that are best able to predict current membrane voltage, and thus indirectly, to predict the current activity of synaptic inputs as well. Thus, whereas the emphasis of the prior art on synaptic plasticity has limited its relevance to the spatial domain, the present invention extends principles of associative plasticity to the temporal domain.

According to an embodiment, anti-Hebbian plasticity of voltage-regulated ion channels selects the ion channel subtypes that best predict and cancel deviations in membrane voltage. In another embodiment, Hebbian plasticity selects those channel types that best predict and amplify deviations in voltage. Application of an anti-Hebbian rule to these channel types would lead to a neuron in which output corresponds to a prediction error, whereas a Hebbian rule would lead to a neuron in which output corresponds to a pattern. Neurons in sensory systems are known to generate outputs resembling prediction errors, which is an efficient way to represent sensory information. Neurons in motor systems are known to generate patterns that are useful in achieving reward-related goals.

In further embodiments, these types of associative plasticity are simultaneously used to select amongst synaptic as well as non-synaptic inputs. In other embodiments, Hebbian plasticity is modified by reward information, which helps to insure that all of a neuron's information is useful in predicting future reward.

BRIEF DESCRIPTION OF THE DRAWINGS

FIG. 1A-1D are illustrations of the conductance and membrane voltage response of a simplified neuron to a square-wave pulse of glutamate, said neuron possessing glutamate-gated cation channels and voltage-gated potassium channels, as known in the prior art;

FIG. 2 illustrates the inputs or information sources to a single artificial neuron, where each arrow indicates the direction of information flow for an individual input according to one embodiment of the invention;

FIG. 3A-3H illustrate the results of a simulation of a single-compartment, graded-potential, Hodgkin-Huxley-type model neuron that selected among different types of ion channels according to Hebbian and anti-Hebbian plasticity rules; and

FIG. 4 is a block diagram that illustrates a computer readable medium according to one embodiment of the invention.

DETAILED DESCRIPTION OF THE INVENTION

A biological neuron is described in order to illustrate how the artificial neuron of one embodiment learns to make predictions.

Biophysics and Prediction Error

A neuron integrates information in the voltage differential across its membrane. A neuron expends energy to maintain a higher concentration of sodium ions on the outside of its membrane, and a higher concentration of potassium ions on the inside. A neuron has pores or channels in its membrane, which differ in the ions that they allow to pass. For example, some ion channels are selective for potassium, and thus when they open, potassium flows down its concentration gradient, exiting the neuron and thereby hyperpolarizing the membrane towards the potassium equilibrium potential, which is usually about −100 mV. Neurons typically have many different types of ion channels, but the simplest neuron that could possibly integrate information in its membrane voltage would have just two types of channels that differ in their ionic selectivity.

Such a simplified neuron contains one set of channels that are permeable to both sodium and potassium, and these channels therefore have an equilibrium potential of zero millivolts (E_(cat)=0). They open in the presence of a sufficient concentration of an external chemical. In this example, the chemical is glutamate, and thus these are glutamate-gated ion channels. The second type of channel conducts potassium when it is open, and it is gated by membrane voltage. The potassium equilibrium potential is −100 mV (E_(K)=−100). The voltage across the neuron's membrane therefore approaches a steady-state value (V∞) of

$\begin{matrix} {V_{\infty} = \frac{{G_{cat}E_{cat}} + {G_{K}E_{K}}}{G_{cat} + G_{K}}} & (1) \end{matrix}$ where G_(cat) and G_(K) are the cation and potassium conductances, respectively.

The response of such a neuron to a square-wave pulse of glutamate is shown in FIG. 1 (prior art). The neuron is depolarized when glutamate-gated channels open, but then it gradually repolarizes as voltage-gated potassium channels begin to open. Information about glutamate concentration therefore flows to glutamate-gated channels, then to membrane voltage, and then to potassium channels. Since voltage is the output of the neuron, the conductance of the potassium channels corresponds to a memory of past outputs.

Both sets of channels contain information about glutamate concentration, and thus they can each estimate or predict glutamate concentration. At each brief moment in time, the conductance of the potassium channels depends only on past glutamate concentrations, whereas the conductance of glutamate-gated channels depends at least in part on current glutamate concentrations. Therefore, the glutamate-gated channels possess current information about glutamate concentration, whereas the potassium channels possess prior information about glutamate concentration. The neuron can therefore be understood as having two predictions of glutamate concentration, one conditional on current information (i.e. class one inputs), and the other conditional on prior information (i.e. class two inputs). The membrane voltage depends on a comparison of the two predictions or sets of information (FIG. 2).

When the estimate of glutamate concentration by the glutamate-gated channels exceeds the estimate made by the potassium channels, the neuron is depolarized. The neuron is hyperpolarized when the opposite is true. When both sets of ion channels have nearly the same information, the membrane voltage is at an intermediate voltage. This is illustrated in FIG. 1, which shows the response of a neuron with only these two types of ion channels to a square-wave pulse of glutamate. The neuron's membrane voltage (FIG. 1B) can therefore be thought of as a prediction error. The neuron is most surprised and most depolarized immediately after the rise in glutamate concentration, corresponding to a positive prediction error. This is due to the mismatch between the conductances of the two channel types (compare FIG. 1C to FIG. 1D). The hyperpolarization that follows the drop in glutamate concentration would correspond to a negative prediction error.

This positive or negative prediction error is referred to below in the claims as a “discrepancy.” Its physical correlate in the preferred embodiment is the voltage across the neuron's membrane, with an intermediate voltage corresponding to zero prediction error. The precise quantitative relationship between membrane voltage and prediction error is assumed to be monotonic, but not necessarily linear. Likewise, references below to maximizing or minimizing prediction error are intended to apply to any process performed on any monotonic function of prediction error or membrane voltage.

The signaling of prediction error is known to have substantial advantages. The principle of only responding to errors in prediction is that there is no need for a neuron to “teach” itself what it already knows, nor is it generally desirable to tell target neurons what they have already been told. The utility of prediction errors has long been recognized in the literature on reinforcement learning and efficient coding. The output of the neuron of FIG. 1 can be described as a prediction error, since the memory of past outputs carried by the voltage-gated potassium channels counteracts the excitation by glutamate-gated channels. However, the typical neurons of artificial neural networks lack non-synaptic ion channels such as these.

In the example given above, glutamate concentration is the neuron's stimulus. A neuron's stimulus is defined here as the part or aspect of the world that the neuron estimates or predicts. A neuron naturally contains information within its biophysical structure, and that information must be about some aspect of the world which is defined here as the neuron's stimulus. As described in detail further below, a neuron's stimulus is defined precisely by the weighted sum of the neuron's first class of inputs. A neuron's stimulus typically varies in its intensity in a nearly continuous manner, but in principle it could instead exists in one of just a small number of possible states. A prototypical neuron receives current information from multiple individual glutamate synapses, and thus its stimulus is the local glutamate concentration summed across these synapses.

In general, a neuron has multiple types of ion channels that contribute prior information. These channels function to predict and cancel the effect of those channels contributing current information. Channels contributing prior information tend to modulate their conductance in a manner that drives membrane voltage towards a midpoint that corresponds to zero error. Thus the neuron's prior information functions to minimize prediction errors. This principle is illustrated in computational models of neurons in the retina.

A neuron can estimate current light intensity in a small region of space simply by expressing photosensors that are spatially localized. However, light intensity under natural conditions displays strong positive correlations between neighboring points in space and time. Thus an alternative means of estimating current light intensity at a small point in space (i.e. the center) would be to use only information from the recent past and from neighboring points in space (i.e. the “surround”). The proposal is that a neuron receives some inputs that contribute current information directly from the point in space that is of interest, and other inputs that contribute prior information from neighboring points in space and time. The neuron compares these two estimates, or sets of information, and its output corresponds to the discrepancy between the two (equation 1) (FIG. 2). This discrepancy is more commonly referred to here as prediction error.

The suggestion that a neuron's output corresponds to prediction error is purely descriptive. The concept of prediction error is useful for understanding the flow of information and the function of the model neuron. The rationale for this term becomes more clear in light of the plasticity rules described below. However, the notion of prediction error places no constraints on the processing performed by a neuron, which is determined purely through well established biophysics, as exemplified by equation 1. Nor does the concept of prediction error place any constraints on the information possessed by a neuron. A neuron's predictions are simply conditional on whatever information the neuron happens to have. In principle, a neuron's prediction could have infinite uncertainty, corresponding to a complete lack of information. However, the plasticity rules described further below would usually allow a neuron to gather relevant information so that the concept of prediction error becomes useful in describing the neuron's computational function

In one embodiment, the output of a neuron corresponds to its membrane voltage. By contrast, most real neurons communicate to other neurons through all-or-nothing action potentials that are triggered when membrane voltage crosses a threshold. In such a case, the output of a neuron at a brief moment in time would be binary. A digitized output represents a loss of information relative to that contained in the analog voltage signal. However, a digitized output is advantageous for reliable communication across longer distances. Many neurons that do not transmit information across long distances do not emit action potentials but signal using a graded membrane potential. The preferred embodiment is based on such a graded-potential neuron. However, it should be clear that the principles of the invention could be implemented instead in a spiking neuron with a binary output.

Selection of Prior Information Sources

The neuron receives multiple individual inputs, each of which contributes information from a different point in space or a different period of the past. Each of these individual inputs functions as a source of information. Somehow a neuron selects some of these information sources and discards other. As described above, the neuron receives two classes of inputs, those contributing current information and those contributing prior information. Current information sources are selected to maximize the neuron's prediction errors (i.e. cause the membrane voltage to approach its limits of hyperpolarization and depolarization), whereas prior information sources are selected to minimize the neuron's prediction errors (i.e. cause the membrane voltage to approach an intermediate value). Although there are multiple means by which this end might be achieved, the neuron of the preferred embodiment does so through Hebbian and anti-Hebbian plasticity.

The inputs that contribute prior information span a spectrum of points in space and time, and a neuron is proposed to select those inputs that best minimize the error in predicting stimulus intensity. Which period of the past a channel represents (its “memory”) depends on its kinetic properties. In the simplest case, a channel's gating kinetics could be governed by a single exponential process, but the gating of real channels typically depends on relatively complex interactions of multiple exponential processes. There are numerous types of non-synaptic ion channels that differ in their kinetic properties as well as in their voltage dependence, with the diversity of potassium channels being particularly striking. Different types of channels carry information from different periods of the past. However, a neuron expresses only a subset of these ion channels. By expressing only a subset of these ion channels, a neuron selects to maintain a memory of some periods of the past but not other periods. It is proposed that the pattern of a neuron's stimulus, acting via the voltage-mediated error signal, would select the types of non-synaptic ion channel, and the corresponding periods of the past, that best predict stimulus intensity. An analogous process would also occur in the spatial domain, where discrete synapses represent discrete points in space. For example, as in the case of the retina described above, an individual input could be an inhibitory synapse representing light intensity in a particular region of the surround (determined by the presynaptic neuron's stimulus, or receptive field center). Those synapses from the surround that best predict stimulus intensity in the center would be strengthened.

To illustrate how this occurs, we again consider a neuron in which the inputs contributing prior information consist only of potassium channels. Now there are distinct types of potassium channels that vary in their kinetic properties. The total potassium conductance (G_(K)) at a given moment in time is the weighted sum of the activities of each component (i) or type of potassium channel. G _(K)=−Σ_(i) w _(i) U _(i)  (2)

The activity of a component (U_(i)) refers to the time- and voltage-dependent likelihood that a channel of that type is open at a given moment (i.e. the channel's open probability in a Hodgkin-Huxley type model of average channel behavior). A component's weight (w_(i)) corresponds to the number of functional channels of that type. The weights could be adjusted by inserting or removing channels from the membrane, or by an event such as phosphorylation that could cause a channel to switch from one functional type to another.

Minimizing the error corresponds to driving the membrane potential towards the middle of its range where the error is zero. In the typical case in which current information sources are depolarizing, depolarized potentials would correspond to positive errors and hyperpolarized potentials would correspond to negative errors. If a depolarization-activated potassium channel is open when the membrane is depolarized (positive error), it is correctly guessing that glutamate concentration is high even though the neuron's prior information sources as a whole guessed too low. Therefore the weight of that type of potassium channel should be increased (made more negative, as specified below in equation 3). If the membrane is hyperpolarized (negative error) when a potassium channel is open, then channels of that type should be removed since they guessed too high and contributed to the negative error. If a potassium channel is closed, it bears no responsibility for whatever the voltage may have been, and its corresponding weight should not be changed substantially. The same principles could be applied to adjusting the weight of a channel type that depolarizes the membrane when it is open and conducting.

These principles suggest a learning rule like the following: w _(t+1) =w _(t) −αU _(t)(V _(t)−θ)−βw _(t)  (3) where the weight (w) of an individual component is updated at each moment in time (t) according to its activity (U), membrane voltage (V), and learning rates (α and β). A weight in this case could be any negative real number. The last term (βw_(t)) would correspond to channels being removed from the membrane at a low rate, which would help to insure that the weight of channel types in which activity is not substantially correlated with membrane potential approaches zero. The term θ refers to a voltage near the middle of the range. It functions as the null point of membrane voltage where there is no error; it could be a constant or it could vary. Depolarization beyond θ would increase weights, whereas hyperpolarization would decrease weights.

Equation 3 is appropriate for potassium channels and others that exert a hyperpolarizing influence on membrane voltage. However, some channel types that contribute prior information may have a depolarizing influence (such as HCN cation channels that are activated by hyperpolarization). The weight of this type of channel should be increased when these channels are open at the same time that the neuron is hyperpolarized, since the channels would then be counteracting the negative error. This would be achieved if the first minus sign in equation 3 (the one furthest to the left) were changed to a plus sign in the case of depolarizing inputs.

Plasticity algorithms such as Equation 3 are often referred to as “anti-Hebbian.” A Hebbian rule strengthens depolarizing or hyperpolarizing inputs that are paired with depolarization or hyperpolarization, respectively, and it therefore involves positive feedback. An anti-Hebbian rule does just the opposite and results in negative feedback. Anti-Hebbian plasticity has previously been proposed to govern the strength of some synaptic connections, in both biological and artificial neural networks. The present artificial neuron extends its application to selecting among non-synaptic ion channels. Within the present framework, a functionally relevant term for an anti-Hebbian rule would be “error minimizing.”

By utilizing anti-Hebbian plasticity to select amongst prior information sources, the neuron described above is able to learn to predict the state of a part of the world. Which part of the world the neuron learns to predict will depend on its current information sources (which define its stimulus). Just as a neuron selects amongst its prior information sources, its also selects amongst its current information sources. This selection process should insure that the neuron's information is about an aspect of the world that is interesting and important.

Selection of Current Information Sources

The neuron described above would learn to predict whatever stimulus provides it with current information. However, real nervous systems are only concerned with aspects of the world that are relevant to future reward. Future reward as used herein is very similar to use of the term in reinforcement learning, in which a key goal is to predict the sum of future rewards. The general function of the nervous system is to predict (i.e. minimize uncertainty about) future reward. Future reward is ultimately defined in terms of biological fitness, or the ability of an animal to perpetuate its genetic information, which is the goal of all life forms. In the case of an artificial neural network, future reward would correspond to the future success of the network in achieving its goals (as defined by the network's designer). Since all of a system's outputs should be selected to promote future reward, all the system's information should be about future reward. The term “reward,” as used herein, refers not only to good outcomes, but rather to a measure of value that ranges from bad to good.

This broad and inclusive concept of future reward is quite abstract and intangible. However, as in reinforcement learning, a system predicts future reward by predicting concrete physical stimuli that are themselves predictive of future reward. These stimuli would include every aspect of the world that can be sensed by the nervous system, where a stimulus could correspond to a part of the external world or to part of the system's internal world. For example, this includes generally weak predictors of future reward such as light intensity, as well as strong predictors such as the sight or taste of food. For a neuron in the motor system, the reward-predictive stimulus could correspond roughly to a plan for action. Thus the current state of the world is not of interest in itself, but rather it is of interest only because it contributes information about the future, and specifically about future reward.

Just as a neuron may select which points in space and time are most informative in predicting stimulus intensity, it may also select the stimulus that is most informative about future reward. A prototypical neuron's proximal stimulus is defined as the glutamate concentration summed across a subset of synapses. Each discrete synapse corresponds to an individual source of current information. The neuron selects its stimulus, or set of current information sources, by giving high weights to some synapses and low weights to others.

There are two criteria that are important in selecting amongst sources of current information. First, those individual inputs (i.e. synapses) in which activity is predictive of established reward predictors (e.g. food) should become strong. If a neuron is to learn on its own which inputs are the best predictors of reward, it would require some form of reward feedback. One example of reward feedback would be the reward prediction error signaled by midbrain dopamine neurons, which integrates a vast amount of the system's information and signals whether the current state of the world is better or worse than expected. Another form of reward feedback could come from the top-down feedback projections that mediate selective attention in the neocortex. A reward feedback signal could be much less sophisticated than these examples, and in the simplest case it would be provided solely by natural selection over generations. In an artificial neural network, reward feedback could be provided either by other neurons in the network, or by an external supervisory signal. As for all aspects of the present model, the neuron simply works with whatever information it happens to have. As described below, relevance to reward is not the only criterion a neuron should use in selecting its class one inputs, and the model neuron does not necessarily require any reward feedback.

The second criterion is that to best predict future reward, a neuron should select the stimulus (i.e. set of class 1 inputs) that is the least predictable given the neuron's prior information. This is similar to the principle in statistics that the greater the variance in one parameter (e.g. light intensity), the greater its potential to explain the variance in another parameter (e.g. availability of water). However, even if the intensity of a stimulus has a high variance, and it is correlated with reward, it is not useful to a neuron if it is highly predictable, since it would merely be telling the neuron what the neuron already knows. The most unpredictable inputs are therefore the most informative. Thus, other things being equal, it is the most unpredictable stimulus that would be expected to provide the neuron with the most information about future reward.

One way in which a neuron could select a stimulus that is both predictive of future reward and unpredictable is through application of a learning rule similar to that given above (Equation 3), but with a sign change and now also including any reward information (R) that might be available: w _(t+1) =w _(t) +αR _(t) U _(t)(V _(t)−θ)−βw _(t)  (4)

The weights (w) in this equation could be any positive real number. If the only feedback about reward is provided by natural selection over generations, then R would be constant over the lifetime of the organism, and this rule would simply tend to select the stimulus that is the least predictable. Although not shown in Equation 3, reward information may also shape the selection of inputs contributing prior information. However, even without a direct influence of reward in Equation 3, the influence of reward in Equation 4 insures that a neuron's prior information is predictive of future reward. The goal of this plasticity rule (equation 4) could also be achieved if weight changes were to depend on the conjunction of presynaptic activity at one moment and postsynaptic activity a short time later, as in the case of spike-timing dependent plasticity.

Equation 4 applies to the prototypical case of inputs, such as glutamate synapses, that are depolarizing. However, if an input has a hyperpolarizing influence, then the plus sign in equation 4 would be changed to a minus sign. This would insure that hyperpolarizing inputs that coincide with hyperpolarization, and thus contribute to negative errors, are strengthened (i.e. their weights are made more negative).

The plasticity algorithm of equation 4 is a Hebbian-type rule, and it tends to maximize the neuron's prediction errors. This type of rule strengthens synapses in which activity tends to be synchronous. Synchronous activation would occur more frequently in a subset of synapses that are driven by a recurring spatial pattern or object in the external world. Those synapses would become strong, thereby shaping the stimulus to which the neuron is tuned.

Although Hebbian plasticity is often utilized in artificial neural networks, the distinct proposal of the present work is that a Hebbian rule functions to maximize errors, and to suggest why this is advantageous in learning to predict future reward, the ultimate goal of the nervous system. An error-maximizing rule insures that the stimulus contributes information that the neuron does not already possess. For example, if a neuron receives a stereotyped temporal sequence of excitatory synaptic inputs, then the Hebbian rule will selectively strengthen the first input in the sequence (since prior information will tend to suppress responses to the latter excitatory inputs). The first input is the sequence is the most informative since it predicts the latter inputs, and it could allow for the network to prepare appropriate behavioral outputs in anticipation of the latter events. Thus the error-maximizing rule explores the external environment to identify the best source of external information about future reward, whereas the error-minimizing rule identifies the internal substrate that is best able to capture and hold that information. They both function together to maximize the neuron's information about future reward.

Although the focus of the above discussion has been on selecting amongst information sources from discrete points in space (i.e. synapses) or discrete periods of the past (i.e. types of ion channel with distinct kinetics), these same rules could also select amongst other aspects of a neuron's ion channels and their modulatory proteins. For example, the neurotransmitter receptors that gate ion channels could differ in their ligand affinity, or they could differ in their rates of desensitization. In a simulation described below, a Hebbian rule selected an ion channel subtype with a ligand affinity appropriate to the actual range of ligand concentrations to which the neuron was exposed. Similarly, voltage-gated potassium channels can differ in their voltage-dependence (even while having similar kinetic properties), and an anti-Hebbian rule could select the one that best predicts and counteracts deviations in membrane voltage. In principle, every input to a neuron could be selected by one of these two types of plasticity rules, regardless of the dimensions across which inputs may vary.

Hebbian and anti-Hebbian plasticity rules are recognized within the prior art to be classes of plasticity algorithms, and the particular algorithms given above in Equations 3 and 4 are intended only as examples of these classes.

What a neuron is capable of learning would obviously depend on the set of information sources that are available to it. In designing an artificial network, the designer would need to choose what information sources are available to each neuron. A neuron could obviously receive an input from every other neuron in the network (even if some inputs have weights of zero), or from only a subset of neurons. Similarly, the designer would need to decide upon the kinetics of a neuron's non-synaptic ion channels, or equivalently, which memory traces of its past outputs are available to the neuron as sources of prior information. The invention places no limitations on the information sources available to a neuron, which would chosen by the designer of a network. For example, the kinetic properties of real ion channels would not constrain the sorts of memory traces that are available to an artificial neuron. Furthermore, the designer could arrange for a presynaptic neuron to supply two inputs to a single postsynaptic neuron. The weight of one of these could be controlled by a Hebbian rule, whereas the other could be controlled by an anti-Hebbian rule. The plasticity rules would determine whether the presynaptic neuron contributes current information, prior information, or neither. The guiding principle is that the neuron works with whatever information sources are available it, and it is left to the designer to determine what information sources will be available to the neuron.

Alternatives to Hebbian and Anti-Hebbian Plasticity

A central tenet of the invention is that some of a neuron's inputs are to be selected to maximize prediction error, whereas others are to be selected to minimize prediction error. Plasticity rules are only one means to achieve this end. Plasticity rules have at least two distinct advantages. First, each weight is modified using only information that is locally available. Thus these rules are be implemented in hardware, including biological systems. Second, plasticity rules are constantly updating the weights, thereby allowing a neuron to continually adapt to a changing environment. These features make it possible for an artificial network to learn for itself, so that it does not need to have information fed into it from an external source. Hebbian and anti-Hebbian plasticity rules are therefore utilized in the preferred embodiment.

In an alternative embodiment of the invention, statistical estimation procedures are used to determine a neuron's optimal input weights. Linear mean squared estimation can be used to determine the best sources of prior information for minimizing error. For example, one can use this technique to select those regions of the surrounding space and those periods of the past in which light intensity is the best predictor of current light in a central region. Whereas this technique is designed to minimize squared errors, an analogous statistical technique could be used to choose the weights of class one inputs (i.e. current information sources) in order to maximize squared errors. Because each weight can be determined using information about all other weights and intensities at many points in space and time, this and other statistical methods could potentially select a set of weights that is closer to optimal than the set of weights obtained by a plasticity rule. However, because such statistical methods do not depend only on local information, this approach may require feeding expert information into the network.

In another embodiment of the invention, the designer of the network could choose a neuron's inputs in accord with the principles described here but without the aid of plasticity rules or statistical techniques. For example, if a neuron's stimulus is the position of an object, then we know that the object has mass and therefore also has inertia. Based on this simple knowledge, and nothing more, a neuron could minimize its prediction error if its sole source of prior information derives from the position of the stimulus in the preceding moment since the most recent past is always a better predictor than the more distant past. Such a neuron would be excited or inhibited when the position of its stimulus is different from its position in the last moment. A plasticity rule or a statistical method may have this same result, but it can be deemed unnecessary in such a case. Thus the principle of minimizing or maximizing the neuron's prediction error is implemented directly by the designer of the network based on available knowledge.

Summary of Embodiment Illustrated in FIG. 2

FIG. 2 illustrates the inputs to a single neuron in the preferred embodiment. Each arrow represents an individual input (i.e. a distinct population of ion channels) and its corresponding direction of information flow. Each input would be either excitatory (i.e. depolarizing) or inhibitory (i.e. hyperpolarizing). The number of individual inputs is not constrained by the invention, and the number shown here was chosen for illustrative purposes only. Each individual input is associated with a modifiable weight that indicates the strength of its contribution to the neuron's membrane voltage. Membrane voltage 200 corresponds to prediction error and serves as the neuron's output. Each individual input is “tagged” according to whether its weight is determined so as to maximize or minimize prediction errors.

The weights associated with a first class of inputs 210 are selected to maximize prediction errors. These inputs are described here as contributing current information, and in the preferred embodiment their weights are determined by a Hebbian plasticity rule. The weights associated with a second class of inputs 220 and 230 are selected to minimize prediction errors. These inputs are described here as contributing prior information, and in the preferred embodiment, their weights are determined by an anti-Hebbian plasticity rule.

Those inputs contributing current information 210 and prior spatial information 220 come from other neurons in the network (i.e. synaptic inputs) or from sources external to the network. By contrast, those inputs contributing prior temporal information 230 come from ion channels regulated by the same neuron's membrane voltage. The activity or conductance of each of these inputs depends on past membrane voltages and influence current membrane voltage. Thus information flows in both directions between membrane voltage 200 and the activity or conductance of these inputs 230. Each individual input contributing prior temporal information corresponds to a type of channel with distinct kinetic properties. A channel's kinetic properties determine which period of the past it remembers, and thus distinct channels contribute distinct prior temporal information (i.e. memories). In one embodiment, the neuron integrates its inputs according to the established biophysical rules that apply to biological neurons (e.g Equation 1).

The Network

The above description is concerned with inputs for a single neuron. A single neuron may have some utility by itself, but it is intended to serve as an information processing element in a network of neurons. In one embodiment, each neuron initially differs only in its spatial location within the network, the sign of its output (i.e. excitatory or inhibitory), and its randomly selected input weights. Through. modification of its weights, the network would learns to achieve its goals.

The prediction of future reward is the central function of the nervous system, and the neuron described above performs this function. A single neuron predicts the state of only a small part of the world, and that part of the world may not be tightly linked to future reward. However, if each individual neuron performs this central function, a system of neurons can be assembled to work together to better predict future reward. Because each neuron is at least roughly similar in its biophysical characteristics, each neuron possesses a similar amount of information about its stimulus. However, some stimuli are highly informative about future reward (e.g. the sight of food), whereas others are only weakly linked to future reward (e.g. light intensity). Thus neurons differ in how much information they have about future reward, and this is the critical variable at the level of the network.

Because reward feedback contributes to the selection of each neuron's stimulus via Equation 4, the stimulus of each successive neuron in a series progressing from the network's sensory inputs to its motor outputs is more closely tied to future reward and less closely related to the immediate sensory world. Neurons further from the sensory periphery therefore have more information and less uncertainty about future reward. This phenomenon can be illustrated by tracing a long path from the retina through the cortex to a motor neuron. In the visual system, the stimulus of successive neurons is transformed from small circles of light intensity to oriented bars and eventually to faces.

Higher neurons in the parietal and prefrontal cortex respond to relevant information, regardless of modality. Further along this path, neurons continue to become more selective for future reward, but they also become more motor by integrating proprioceptive and vestibular information specifically related to particular limbs and muscles. As the last neuron in the path, the stimulus predicted by a motor neuron would correspond roughly to a plan for action. Because the cumulative effect of reward feedback at every upstream synapse shapes the motor neuron's stimulus, the motor neuron has less uncertainty about future reward than any of its upstream neurons. Likewise, the motor neuron renders the system's decision.

The amount of reward information possessed by a neuron and its stimulus also varies across sensory modalities. For example, because taste is more strongly correlated with future reward than is light intensity, a gustatory cell in the tongue has more information and less uncertainty about future reward than does a photoreceptor. Likewise, a gustatory cell is closer to motor neurons (i.e. separated by fewer synapses) than a photoreceptor. If a gustatory path and a visual path both converge upon the same motor neuron, then they produce the same reduction in uncertainty about future reward. However, because light intensity is a lesser predictor of future reward, the long path of the visual system must do more work than the short path of the gustatory system in order to cause the same reduction in reward uncertainty. However, in doing substantial work to extract reward information from light intensities, the long path of the visual system achieves a much greater reduction in uncertainty about the world in general.

The ability of a network of these neurons to learn to generate an intelligent and useful output is largely dependent on the presence of one or more reward feedback signals. In one embodiment, the appropriate form of reward feedback is not specified. Rather the artificial neuron makes use of reward feedback so that the network's information is relevant to its goals. In the absence of reward feedback, a network of these neurons learns to predict the state of aspects of the world that are difficult to predict. For example, such a network might learn to see, to understand and predict the visual world. It could learn to recognize objects, but unlike a biological system, it does not view some objects as more important than others. Such a network is informative to an external observer, and thus is useful, but is not suitable for generating goal-related motor outputs that resemble those of a biological system.

A critical issue in designing a network of these neurons concerns the form or forms of reward feedback. ‘Reward feedback’ refers to information about how well the network's goals are being achieved. Through its influence on Hebbian plasticity, as indicated in equation 4, this reward feedback will determine the information that a neuron and a network acquire. Reward feedback helps to insure that all of the network's information is relevant to the network's goals. The form of reward feedback is not specified here, although several examples have been provided above. It could come from special neurons within the network that, rather than being simply excitatory or inhibitory, have a modulatory effect analogous to the neurotransmitter dopamine. Alternatively, it could be provided from a source external to the network, in which case the network would be said to learn in a supervised manner. Thus there are multiple embodiments that differ in their reward feedback. A critical aspect of these neurons is that they are able to make use of whatever reward feedback is provided in order to predict those aspects of the world that are most relevant to the network's goals.

Biological neural networks are only concerned with those aspects of the world that are of potential relevance to an animal's goals. But one can imagine an artificial network that is interested in predicting the state of the world in the absence of any specific behavioral goal (i.e. understanding just for the sake of understanding). Thus, in one embodiment, no reward feedback is provided. To imagine how such a network might function, a useful analogy may be drawn to the visual system. Later stages of the visual system are strongly biased in favor of reward relevant information. Under the influence of reward feedback, the visual system learns to perform detailed processing of faces, while largely ignoring objects such as rocks. But the early visual system learns recognize and discriminate all sorts of objects, regardless of their relevance to reward. A network of these neurons that learns in the absence of reward feedback would likewise be expected to recognize and discriminate objects. For example, it has been shown that Hebbian plasticity could cause neurons to become selective for elongated regions of contras. Hebbian plasticity could therefore account for the stimulus selectivity of simple cells of primary visual cortex. Thus a network that lacks reward feedback might be capable of learning to see (i.e. predict the state of the visual world).

Simulation

In one embodiment of the invention, a network of one or more neurons is simulated using a computer. The results of such a simulation are presented herein.

Previous studies have demonstrated how Hebbian or anti-Hebbian synaptic plasticity rules could shape a network (although the proposed combination of both rules has not been simulated). An embodiment of the present invention extends the application of these same sorts of plasticity rules to the selection of non-synaptic ion channels. In this simulation a single neuron selected from amongst a spectrum of non-synaptic ion channels, as shown in FIGS. 3A-H.

The simulation is based on a single compartment, graded potential (i.e. no action potentials), Hodgkin-Huxley type model neuron. The neuron simultaneously selected from among four subtypes of glutamate-gated cation channels through a Hebbian rule (Equation 4), and from among nine subtypes of voltage-regulated potassium channels through an anti-Hebbian rule (Equation 3). Channel activity (i.e. open probability, “U” in equations 2-4) varied continuously between 0 and 1, as shown in FIGS. 3C, 3E, and 3G. The number of channels of each type (i.e. “w” in equations 2-4) could assume any positive real number. The unit conductance of each channel was one.

For the plasticity rules of equations 3 and 4, θ was chosen to be −50 mV, midway between the potassium and non-selective cation reversal potentials. The rate constant α was 0.1 and 1.0 for the anti-Hebbian rule of equation 3 and the Hebbian rule of equation 4, respectively. For each rule, β was 0.0000001. Besides the particular pattern of glutamate concentration, the plasticity rates were the only free parameters in the simulation. Other parameters were chosen either to approximate known physical values or, in the case of channel subtypes, to span a spectrum of relevant kinetics or glutamate affinities. The greater value of α in the anti-Hebbian rule relative to the Hebbian rule was chosen to constrain growth in the number of glutamate-gated channels resulting from the positive feedback of the Hebbian rule (by making the negative feedback of the anti-Hebbian rule faster). The “passive” decay rate (β) was chosen to be much less than the “active” plasticity rate (α), which in turn was chosen to be slow in comparison to the rate of change in channel activities.

At each time step, glutamate concentration was drawn from a Gaussian distribution with a standard deviation of 20% of the mean, as shown in FIG. 3A. The mean concentration increased from 50 to 1000 μM for ten time steps starting at 2000, and again for 500 time steps starting at 2200. After 5000 time steps the pattern repeated, for a total of 20,000 cycles. Initially, there were a total of 800 glutamate-gated non-selective cation channels, evenly divided among four subtypes, and 800 voltage-gated K+ channels, evenly divided among nine subtypes. Two other simulations began with different numbers and proportions of channels (not shown). The final numbers of channels of each subtype were the same in all three simulations, regardless of the starting numbers.

The four types of glutamate-gated channels differed in their affinities (K_(D)) for glutamate. This can be seen in FIG. 3C, which shows the activities (i.e. open probabilities) for each channel type during a single cycle. Subtypes with intermediate affinities were the most sensitive to the actual range of glutamate concentrations to which the neuron was exposed. Their activity was more variable and less predictable, and one of these (K_(D)=1000 μM) was therefore the predominant subtype selected by the Hebbian plasticity rule of Equation 4. FIG. 3D shows the numbers (i.e. weights w in Equation 4) of each type of glutamate-gated channel as a function of cycle number, where the value for each cycle was the average weight over all 5000 time points in the cycle. The Hebbian plasticity rule selected the most advantageous channel types, those that maximized prediction errors or deviations in voltage, and disposed of the others. As learning progressed and higher and lower affinity receptors were eliminated (FIG. 3D), the neuron's membrane potential became more sensitive to glutamate concentration and therefore more variable. This is illustrated in FIG. 3B, in which the bottom trace showing membrane voltage during the last cycle is highly variable in comparison to the top trace showing membrane voltage during the first cycle.

The neuron's prior information (i.e. class 2 inputs) comprised 9 subtypes of potassium channels. Four of these were type 1 and five were type 2 channels. Type 1 channels were gated by a single two-state voltage sensor with a half-maximal activation at −40 mV at equilibrium, and thus their activity at each moment was simply an exponential function of past voltages. The activities of each type of channel are shown in FIG. 3E during the last cycle. The four subtypes differed in their kinetic properties, with time constants τ at −40 mV ranging from 10 to 333 time units. For approximately the first 1000 cycles, the number of each type of potassium channel increased from its starting value of 89 because the membrane voltage was almost always depolarized beyond θ (−50 mV) in equation 3. This continued until the total potassium conductance was sufficient to bring the membrane voltage near the null point θ where the average error was zero. The anti-Hebbian rule of equation 3 ultimately selected the channel type with the fastest kinetics (τ=10 time points), as shown in FIG. 3F. This channel was appropriate in this case because the most recent past was better than the more distant past in predicting membrane voltage, and thus in predicting glutamate concentration as well. This was true both because of the short range correlations in membrane voltage introduced by the membrane time constant, which for simplicity was fixed at one time unit, and because of the step changes in mean glutamate concentration. The channel with the fastest kinetics was able to more rapidly adapt its prediction and thereby minimize the error. Indeed, many real voltage-gated potassium channels have fast kinetics. However, the most recent past is not always the best predictor of the present. Likewise, when glutamate concentration displayed Gaussian variation but lacked other temporal patterns, the anti-Hebbian rule selected the channel type with the slowest kinetics, since that channel made the best predictions by averaging over the longest period of past voltages (not shown).

The type 1 potassium channels were not able to predict when the second pulse of glutamate would occur given the first pulse, but in principle, some types of channel could do so. The type 2 potassium channels were designed for this purpose. Each of the five subtypes of type 2 potassium channel were gated by eight sensors, as previously described. The subtypes differed in their kinetic properties as shown in FIG. 3G. The gating of each type 2 channel by multiple sensors made it more like real channels relative to the single-sensor type 1 channels. The rules of channel gating and sensor kinetics were chosen so that a channel opened for a certain time period after membrane voltage was depolarized beyond −25 mV. For nearly the first 2000 cycles, this threshold was never reached, and thus the number of each subtype of type 2 channel declined due to the passive decay term of equation 3 (FIG. 3H). Eventually, as membrane voltage became more sensitive to glutamate concentration due to the selection of more sensitive glutamate-gated ion channels, the first pulse of glutamate became sufficient to depolarize the membrane beyond −25 mV and thereby activate type 2 channels. Thereafter, the anti-Hebbian rule selected the channel subtype with kinetics that roughly matched the actual interval between the two pulses of glutamate (τ=100) (FIG. 3H). This subtype was selected because it counteracted the glutamate-driven depolarization (i.e. positive error), and in spite of the fact that it also caused a brief hyperpolarization (i.e. negative error) prior to the second pulse of glutamate (FIG. 3B, bottom trace). Thus this type of channel could use the first pulse of glutamate to predict and counteract the depolarization caused by the second pulse of glutamate.

The function of a neuron would depend on the information sources (i.e. channel types or synapses) available to it. This example is provided only for illustration and is not meant to limit the sorts of information sources that could be available to a neuron.

Computer Readable Medium

In one embodiment, the artificial neurons are generated using a software program stored on a client 400. FIG. 4 is a simplified diagram that illustrates an exemplary architecture for generating a network of artificial neurons. The exemplary architecture is a client 400 (e.g. a computing platform configured to act as a client device such as a computer), a digital media player, a personal digital assistant, or a cellular telephone that is configured to include a computer-readable medium 410, such as random access memory (RAM) or magnetic or optical media, coupled to an electronic processor 420. The processor 420 executes program instructions stored in the computer-readable medium 200.

Using Hebbian Plasticity to Select Amongst Voltage-Regulated Ion Channels

The invention described hereinabove was based on a model of the function of a single artificial neuron. Hereinbelow, most of the ideas are the same as or similar to hereinabove, but the invention should be understood as specifying particular types of inputs to a neuron and the plasticity rules that regulate the weights of those inputs. The invention does not fully specify the features of an artificial neuron. Thus embodiments of the invention could include additional inputs to a neuron and their regulation by plasticity rules that are not specified herein.

The ideas described hereinabove include how the nervous system can learn to predict important aspects of the world (“future reward”) using information that comes from the sensory environment. However, such information can also be internally generated.

The nervous system is capable of generating patterns that do not have any direct dependence on patterns in the sensory environment. Patterned motor outputs are generated at early stages of development, prior to the time during development that sensory neurons provide information to the nervous system. Likewise, some neurons generate patterned outputs in the absence of any patterned synaptic input. These neurons, or the networks in which they are found, are sometimes called central pattern generators (CPGs). CPGs are known to be important in motor systems, particular those that generate relatively simple, sine-wave-like output patterns, as in swimming, walking, and respiration. Hereinbelow, the principles found in the original application are modified in order to account for pattern generating neurons.

However, the more general and fundamental principle underlying this extension of the original technique is that information can originate within the nervous system, and within single neurons, rather than coming from external sensory inputs. Sensory information, which by definition originates from sources external to the nervous system, is useful because it can be predictive of “future reward.” However, internally generated information could also serve this same purpose. First, this would require that the nervous system intrinsically generates patterns, which are defined here as any time-varying output, a simple example being a sine wave. Second, just as in the case of sensory patterns described hereinabove, the system would require a sensory-dependent reward feedback signal to select those patterns that are predictive of future reward. Hereinbelow is described how this could occur by introducing a small but important variation to the technique described hereinabove.

To illustrate the present ideas, it is useful to imagine two types of neurons. The neuron described hereinabove will now be referred to as “type A,” and it is thought to correspond to a neuron of a sensory system. The second type of neuron, which is introduced hereinbelow, will be referred to as “type B” and is thought to correspond to a neuron in a motor system. The fundamental difference between the two types is only in the sign of the plasticity rule (Hebbian versus anti-Hebbian) that determines which voltage-regulated ion channels a neuron expresses. There are reasons why it may be advantageous to apply each type of rule to different types of voltage-regulated ion channels within the same neuron. Thus type A and type B neurons should be understood as exemplary embodiments representing the two extremes, and additional embodiments could consist of mixtures of these two extremes.

It is important to distinguish the method of information processing that constitutes the present invention from neurons, which are only properly defined within biology. A general term that encompasses biological neurons as well as artificial entities is an “information processing element.”

As in the technique described hereinabove, the preferred embodiment is based on a biological neuron in which inputs correspond to ion channels that vary in their conductance and the output corresponds to voltage across the neuron's membrane. Inputs are selected to maximize or minimize the discrepancy between membrane voltage and an intermediate voltage that serves as a homeostatic reference point. In an embodiment consisting of a non-spiking neuron, “the discrepancy” is defined as a monotonic function of the difference between membrane voltage and an intermediate reference voltage. In an embodiment consisting of a spiking neuron, the discrepancy may instead correspond to an increase or decrease in firing rate relative to a homeostatic reference firing rate.

The “activity” of an input corresponds to the fraction of channels of a given type that are open at a particular moment in time, or the channel's open probability in a Hodgkin-Huxley-type model. For convenience, the activity would be a number within the bounds of 0 and 1. The activity of a class 2 input is defined in general as “corresponding to a weighted sum of past outputs of said processing element.” In an embodiment based on a real neuron, a single class 2 input would correspond to a single subtype of voltage-regulated ion channel. The activity of the channel would be a function of past voltages (outputs), as determined by the voltage- and time-dependence (kinetics) of the channel. It should be appreciated that the activity at each brief moment in time would have no dependence on current voltage, because a single time step, corresponding to one iteration of the method of claim 1, is very brief relative to the kinetics of the channels. The voltage- and time-dependence fully determine which period of the past the channel represents, as well known in the prior art. However, it is not simple to state precisely which period of the past determines a channel's activity, because a channel's kinetics (time-dependence) are themselves dependent on voltage. For this reason, the precise “period of the past” that a particular channel type represents varies depending on the past voltage trajectory of the membrane. If the period of the past is described by using a weight for each moment in the past, and then taking a weighted sum of past voltages (outputs), the set of weights for a particular channel type will themselves vary over time. Thus, although it is possible to describe a channel's activity as a weighted sum of past outputs, it is not the most convenient description. More convenient descriptions are provided in the prior art for the time-dependence of voltage-regulated ion channels. However, the description herein of activity corresponding to a weighted sum of past outputs can be convenient for the designer of an artificial neuron. For example, a designer might endow an artificial neuron with a class 2 input in which activity depends only on the value of the neuron's output at past time steps (or iterations) −7, −14, and −21, with no dependence on any other past time steps. Thus those past time steps would have positive weights, and all other past time steps would have weights of zero. While this may be contemplated in an embodiment of an artificial neuron, real ion channels are not known to exhibit this sort of behavior. An ion channel's activity is typically more strongly dependent on recent voltage than on voltages that occurred in the more distant past. The activity of a type 2 input in an artificial neuron could depend on any combination of past outputs, and is not constrained by the time-dependence actually observed in biological ion channels. The weights simply provide a flexible way of describing the dependence on past outputs. It should be appreciated that these weights are completely different from, and independent of, the weights that are modulated by Hebbian and anti-Hebbian plasticity rules.

As described hereinabove, a neuron's inputs were divided into two classes referred to as class 1 and class 2, where class 2 consisted of two subclasses: synaptic inputs contributing prior spatial information and voltage-regulated inputs contributing prior temporal information. However, to promote clarity, a neuron's inputs are hereinafter divided into additional classes. As hereinabove, class 1 inputs are synaptic inputs and are selected in order to maximize the discrepancy in the neuron's membrane voltage. Class 2 inputs are voltage-regulated ion channels that provide prior temporal information. Class 3 inputs hereinbelow include synaptic inputs contributing prior spatial information. Class 1, 2, and 3 inputs are shown in FIG. 2, where they are labelled ‘current information 210,’ ‘prior temporal information 230,’ and ‘prior spatial information 220,’ respectively. Class 4 inputs are “leak” channels that are always open, irrespective of membrane voltage or synaptic activity. The activity of a class 4 input is thus constant over time (over iterations).

In a type A neuron, class 2 inputs are selected (weights are assigned) to minimize the discrepancy, whereas in a type B neuron, class 2 inputs are selected to maximize the discrepancy. That is the only difference between type A and type B neurons. In further embodiments, a neuron may be a mixture of type A and type B, in which case the weights of some class 2 inputs would be assigned to minimize the discrepancy, whereas other weights would be assigned to maximize the discrepancy.

Because a type A neuron only generates an output when its prior information fails to accurately predict the intensity of inputs contributing current information, its output, or membrane voltage, can be described as a ‘prediction error,’ as indicated in FIG. 2. The generation of the prediction error is ultimately the result of selecting prior information sources through anti-Hebbian-type plasticity. Because type B neurons utilize Hebbian plasticity, they predict and amplify the weighted sum of the activity of their class 1 inputs, rather than predicting and canceling, as a type A neuron does. Thus it is not appropriate to refer to the output of a type B neuron as a ‘prediction error.’ A type B neuron could instead be referred to as a ‘pattern generator,’ since it amplifies and promotes patterns that are present in its synaptic inputs.

In some embodiments, the weights of class 1 and class 3 inputs may not be assigned in any principled manner. But in some embodiments, the weights of class 1 inputs would be assigned to maximize the discrepancy. And in some embodiments, the weights of class 3 inputs would be assigned to minimize the discrepancy.

Different methods might be used to select a neuron's inputs so as to maximize or minimize the discrepancy in the neuron's output. However, the embodiments described herein utilize the methods of Hebbian-type and anti-Hebbian-type plasticity rules to maximize and minimize the discrepancy, respectively. Thus the difference between type A and type B neurons is a difference in the sign of the plasticity rule (anti-Hebbian versus Hebbian, respectively) that governs the selection of inputs (through the assigning of weights) contributing prior temporal information (class 2 inputs).

According to embodiments described hereinabove, neurons have prior information that functions to predict and cancel incoming sensory information. In these type A neurons, which may correspond to sensory neurons, an anti-Hebbian-type plasticity rule selects the prior information sources that best predict and cancel sensory inputs. The synapses or ion channel subtypes that tend to bring the neuron's membrane voltage (or firing rate) towards an intermediate, homeostatic level are strengthened, whereas those synapses or ion channel subtypes that drive the neuron away from this homeostatic level of activity are weakened. It is appropriate to call discrepancies in membrane voltage in type A neurons “prediction errors,” because such discrepancies approximate the difference between the prediction of stimulus intensity (the weighted sum of class 2, 3, and 4 activities, which provide prior information) and the actual stimulus intensity (the weighted sum of class 1 activities, which provide current information). Thus, in this scenario, an anti-Hebbian plasticity rule functions to minimize prediction errors. A type A neuron performs what could be called “predictive homeostasis.” Its output signals only what's new (information that was not already in the neuron). The temporal patterns of a type A neuron's output are generally less predictable, and have a less robust pattern, than its class 1 synaptic input due to the effect of anti-Hebbian selection of prior information sources. The temporal prior information (class 2 inputs) of a type A neuron therefore acts to partially remove or filter predicted sensory patterns from the neuron's output.

In an embodiment of a type B neuron, temporal patterns can be generated by selecting sources of prior temporal information to predict and amplify rather than predict and cancel patterns in synaptic inputs. To illustrate the idea, consider the case of a neuron with no synaptic inputs. It is known in the art that the membrane voltage of some neurons oscillates in the absence of synaptic input due to particular combinations of voltage-regulated ion channels and that such neurons are the source of the patterns of CPGs. A neuron such as this exhibits pacemaker properties and typically generates oscillatory bursts of one or more action potentials. For example, a mechanism that has been observed to generate oscillatory bursts in some neurons relies on low-voltage-activated, T-type calcium channels and a calcium-activated potassium channel. The calcium channels cause depolarization of the membrane for about 100 ms, typically leading to several conventional sodium-based action potentials. The membrane eventually hyperpolarizes due to inactivation of T-type channels and activation of calcium-activated potassium channels. Intracellular calcium concentration then declines, causing the potassium channels to close and thereby leading to a depolarization that once again activates T-type calcium channels to initiate another depolarized phase. By such a mechanism, a neuron can generate a patterned output even though it receives no pattern in its synaptic input.

To intrinsically generate oscillations, a neuron must have ion channels with appropriate voltage dependence and kinetics. In an embodiment of a type B neuron, such combinations of channels are selected by utilizing a Hebbian-type rule to assign weights to various types of voltage-regulated ion channels (class 2 inputs). Those voltage-regulated ion channels that contribute to the discrepancy are selected (given high weights), whereas those voltage-regulated ion channels that counteract the discrepancy are weakened and eventually eliminated. As defined here, a Hebbian-type rule strengthens ion channel subtypes that contribute to depolarizing or hyperpolarizing the neuron's membrane voltage at the same time (or just before) the membrane is depolarized or hyperpolarized, respectively. Thus a potassium channel that is open at the same time (or just before) the membrane is hyperpolarized would have its weight increased (by increasing the number of function channels of that type) by a Hebbian-type rule. If the same channel type were open when the membrane is depolarized, that channel type counteracted the discrepancy and its weight would therefore decrease. Thus, a Hebbian-type rule causes a neuron's membrane voltage to tend not to be at an intermediate value.

One potential outcome of a Hebbian rule is that a neuron's voltage becomes constantly depolarized or hyperpolarized relative to the intermediate level. However, a variable output is desirable in the case of a type B neuron. This problem can be overcome by using anti-Hebbian plasticity to select amongst other sources of prior information (synapses or ion channels corresponding to class 2 or 3 or 4 inputs). For example, an anti-Hebbian rule could determine the number (density) of leak channels (channels that are always open and therefore have constant activities; these inputs are referred to herein as ‘class 4’). If the anti-Hebbian learning rate is fast relative to the Hebbian learning rate, then the anti-Hebbian rule functions to maintain the average membrane voltage at the homeostatic level. However, because of the Hebbian rule, the membrane voltage is not stable at this intermediate level. Rather the membrane voltage spends much of its time in a depolarized “UP” state or a hyperpolarized “DOWN” state. Anti-Hebbian plasticity could also be useful for preventing membrane voltage from becoming too depolarized (or firing rates from becoming too high) during the UP state. Thus anti-Hebbian plasticity, or other methods of minimizing variation in a neuron's output, may have an important role in type B neurons as well as type A neurons.

A neuron in which membrane voltage is usually in a depolarized UP state and a hyperpolarized DOWN state is known in the art to display “bistability.” A well known example of neurons displaying bistability is the medium spiny neurons of the striatum. A neuron in which membrane voltage oscillates in a sine-wave like pattern is not usually said to display bistability. However, a useful definition of bistability is a pattern of voltages such that a histogram of voltages has a bimodal distribution with a minimum at intermediate values and maxima at depolarized and hyperpolarized potentials. By this definition, a sine wave pattern is considered bistable. A pacemaker pattern may or may not be considered as bistable, depending on the frequency distribution of voltages. The Hebbian-type rule of a type B neuron will tend to promote variance in membrane voltage across time, and thus it would promote pacemaker patterns and other oscillatory patters, as well as bistability.

Pattern generation would be promoted by Hebbian plasticity at some channel types. For example. Hebbian plasticity at a depolarization-activated calcium channel would promote pattern generation under most circumstances. But an oscillatory pattern may also depend on depolarization-activated potassium channels that function primarily to repolarize the membrane. These channels would typically be weakened by a Hebbian rule, but strengthened by an anti-Hebbian rule. Pattern generation may be facilitated by applying a Hebbian rule to some ion channel subtypes while maintaining anti-Hebbian plasticity at others.

There are many combinations of ion channel subtypes that can generate bistability and many other combinations that cannot. A Hebbian rule would be expected to bias the selection of ion channels in favor of those combinations that generate bistability. However, there are many different output patterns (UP state durations, for example) that are consistent with bistability, but a Hebbian rule would not necessarily bias the neuron towards any particular such pattern. Three factors are described hereinbelow that influence which specific channels a neuron expresses and thus which specific patterns the neuron generates. One factor is the pattern of synaptic excitation and inhibition that a neuron receives, a second factor is the modulatory effect of reward feedback, and a third factor is the influence of the initial conditions.

The influence of the initial conditions can be illustrated by considering a neuron with no synaptic inputs. Through Hebbian plasticity, such a neuron can learn to generate a pattern by selecting a particular combination of ion channels. The ‘initial conditions’ refers here to the particular combination of ion channels that are present in a neuron before Hebbian-type plasticity has taken effect. Because Hebbian plasticity has a winner-take-all property, the initial conditions have a strong influence in determining which ion channels are ultimately expressed. For example, if a T-type calcium channel with slow kinetics is strongly expressed under the initial conditions, then such channel is likely to remain strong or become stronger because it has a strong driving influence on the voltage and its open state therefore tends to be coincident with depolarization. A faster T-type calcium channel would be less synchronized (less in phase) with the slow depolarization created by the slow T-type channel, and thus it would not gain dominance. A slow calcium-activated potassium channel might be selected though Hebbian plasticity in this neuron because its activity would be mostly out of phase with that of the T-type channel and it would therefore drive strong hyperpolarizations. By contrast, a faster potassium channel would be more in phase with the depolarization and would thus counteract the depolarization rather than drive a hyperpolarization. The weight of the fast potassium channel would therefore be decreased. There may be variation from one neuron to another in the initial conditions, and thus a population of neurons could display a great diversity of patterns.

Some patterns may be useful because they help an animal to obtain reward. These patterns are therefore predictive of future reward, and likewise, neurons that generate these patterns posses information about future reward. Many other patterns are not associated with reward and are not useful. It would be desirable that the system possesses a means by which to promote those patterns that are predictive of reward and to eliminate the others. In a further embodiment, such means is achieved by adjusting the types of ion channels in a neuron according to a 3-term Hebbian-type plasticity rule in which the third term is reward information, as in equation (4), which is reproduced hereinbelow: w _(t+1) =w _(t) +αR _(t) U _(t)(V _(t)−θ)−βw _(t)  (4)

It should be appreciated that in this embodiment of a type B neuron, the term ‘ U’ can represent the activity of a particular type of voltage-regulated ion channel (a class 2 input) or an individual synaptic input (a class 1 input), whereas ‘ U’ as used hereinabove for a type A neuron represented only the activity of an individual synaptic input (a class 1 input). ‘R’ represents reward information provided by a modulatory input such as dopamine. High levels of extracellular dopamine signal positive reward. According to a 3-term Hebbian rule, a sodium or calcium channel subtype that is open at approximately the same time that the neuron is depolarized and dopamine receptor activation is high would be strengthened (its weight increased), whereas a potassium channel subtype open at that same time would be weakened. In some embodiments, a decrease in dopamine levels may signal a negative reward event. If R takes negative values, then a depolarizing channel that is open at the same time that the neuron is depolarized and R is negative would have its weight decreased.

Thus according to an embodiment, through a plasticity rule such as this a single neuron could learn to generate outputs that predict reward by selecting voltage-regulated ion channels that predict reward. The diverse temporal or kinetic properties of the ion channels may provide a way of generating a variety of patterns that are internally, rather than receiving patterns from the external sensory world. However, it should be appreciated that the reward signal depends on sensory feedback. Thus, the particular ion channels and patterns that a neuron exhibits after a period of reward-modulated learning depend on patterns in the external world.

As discussed hereinabove regarding the case of synapses, the coincident events that drive Hebbian plasticity would not need to occur at exactly the same time. The principle is that the opening of the ion channel contributes to the depolarization (or hyperpolarization) of the neuron (which would occur a few milliseconds after channel opening, due to the membrane's capacitance), which in turn contributes to the generation of the reward signal (which would necessarily occur with some delay after the neuron's depolarization, if the depolarization of that neuron had a causative effect in obtaining reward). Thus it would be desirable in an embodiment to account for these delays in the chain of causally related events.

In an embodiment, accounting for such delays is achieved by the use of eligibility traces, which is a “memory” that decays over time. Until its eligibility trace has fully decayed, an individual input (a synapse or type of ion channel) is ‘eligible’ for plasticity and learning if a second event occurs, such as depolarization or an action potential. According to such embodiment, the opening of an ion channel leaves an eligibility trace that persists for a short time after the channel has closed (one membrane time constant could be an appropriate duration). The coincidence of that eligibility trace with the depolarization (or hyperpolarization) of the neuron may be detected and then generate a second eligibility trace. The coincidence of the second eligibility trace with the reward signal causes a change in the weight or strength of that type of ion channel by adding or removing functional channels of that type. This is analogous to the case of “spike-timing dependent plasticity” at synapses, which typically employs a 2-term Hebbian rule. For example, the first eligibility trace could be the binding of glutamate to NMDA (N-methyl D-aspartate) receptors, which may last about 100-200 ms, and the second eligibility trace could correspond to the phosphorylation state of calcium-calmodulin dependent protein kinase 2. The first trace would thus represent presynaptic activity, whereas the second trace would represent the coincidence of pre- and post-synaptic activities. The reward signal could be mediated by dopamine activating D1 receptors and thereby modulating protein kinases or phosphatases. As described by Izhikevich for the case of synaptic plasticity (“Solving the distal reward problem through linkage of STDP and dopamine signaling” Cerebral Cortex 17: 2443-2452 (2007)), a mechanism such as this could solve “the distal reward problem.” The more general point herein is that if the activity of a channel or a synapse contributes to a neuron's output, the activity should occur slightly before that output, and if the coincidence of a neuron's input and output activities contributes to generating a reward signal (such as dopamine), then that coincidence should occur before the reward signal. It should be appreciated that the use of eligibility traces is a variation on the Hebbian-type plasticity that has already been discussed hereinabove. Hebbian-type plasticity is recognized in the prior art to include eligibility traces and related phenomena such as spike-timing-dependent plasticity.

As discussed hereinabove, a type B neuron's Hebbian selection of voltage-dependent ion channels depends on initial conditions and on reward feedback. A third important factor is the patterns of synaptic input experienced by the neuron. The inputs that a neuron selects through associative (Hebbian or anti-Hebbian-type) plasticity rules depend on the temporal pattern of its outputs (membrane voltages or firing rates). Because the output is a function of the sum of all of its inputs, and each input in the model neuron is being selected by associative rules, the particular synaptic inputs that the neuron selects depend on the voltage-dependent ion channels that it expresses, and vice versa. Thus, if the plasticity rules for different classes of inputs are implemented simultaneously in an embodiment, there will be a dynamic interaction between selection of voltage-dependent ion channels and selection of synaptic inputs.

Consider the simpler situation of a neuron in which plasticity only acts at voltage-regulated ion channels (class 2 inputs) but not at synaptic inputs (class 1). For example, a type B neuron may receive a strong synaptic input that has a sine wave pattern, and therefore the membrane voltage also exhibits a sine wave pattern. According to a Hebbian rule, the weights of voltage-regulated ion channel subtypes that amplify and promote this sine wave are increased, whereas the weights of those channels that counteract the sine wave are decreased. Once the neuron has learned to recognize the synaptic pattern, the neuron oscillates approximately in phase with and at the same frequency as the synaptic input, assuming that the neuron is capable of expressing ion channels with the appropriate kinetics and voltage dependence. With an appropriate level of constant current injected into the neuron, the neuron may exhibit similar oscillations even in the absence of any patterned synaptic input. The neuron has therefore learned to internally generate the synaptic pattern to which it was exposed. In the presence of the patterned synaptic input, the voltage-regulated ion channels of a type B neuron predict and amplify the synaptic current. By contrast, an anti-Hebbian rule (in a type A neuron) selects those voltage-regulated ion channels that predict and counteract the sine wave pattern of the synaptic input. Thus, after a period of training, a type A neuron is also capable of generating oscillations in membrane voltage that resemble the pattern of oscillations in the synaptic input. However, in the presence of the sine wave pattern of synaptic inputs, the internally generated oscillations of the type A neuron are mostly out of phase with the synaptic input, and therefore function to remove or filter the synaptic sine wave input from the output of the neuron. Thus the voltage-regulated ion channels of a type A embodiment of a neuron implement predictive homeostasis, and voltage-regulated ion channels of a type B embodiment of a neuron implement predictive amplification.

Consider the converse situation in which a neuron's voltage-regulated ion channels are not plastic, but its synaptic inputs are regulated by a Hebbian-type plasticity rule. Because of its particular combination of voltage-regulated ion channels, a neuron may oscillate at a particular frequency. Those individual synaptic inputs that depolarize the neuron at the same time that the neuron is depolarized would increase in weight relative to other synaptic inputs. The neuron would therefore select class 1 synaptic inputs that match its intrinsically generated pattern of membrane voltages. One could say that the neuron has thereby selected synaptic inputs that match its prediction.

Type A neurons are envisioned as predominating close to the sensory periphery, whereas type B neurons are envisioned as predominating close to the motor periphery. Thus, a key difference between sensory neurons and motor neurons may be the sign of the plasticity algorithm (anti-Hebbian versus Hebbian) that selects the voltage-regulated ion channels of the respective neurons.

Although the principles of the invention were well described in verbal form hereinabove and in the published paper (Fiorillo, 2008), the formal mathematical description was not as general as it could have been. As pointed out hereinabove, the anti-Hebbian plasticity of equation 3 was intended to apply to hyperpolarizing inputs (such as potassium channels) and the Hebbian plasticity of equation 4 was intended to apply to depolarizing inputs (such as sodium channels). However, as also stated hereinabove, the invention allows both Hebbian and anti-Hebbian-types of plasticity to be applied to both hyperpolarizing and depolarizing types of channels. Furthermore, although in the preferred embodiment weights correspond to the number of functional ion channels of a particular type, in some cases weights were given negative values, which is counterintuitive.

In the new mathematical formalism described hereinbelow, all weights are positive real numbers. Thus, equation 2 becomes G_(K)=Σ_(i)w_(i)U_(i)  (5) which is the same as equation 2 but without the minus sign. The term ‘z’ is introduced here, and its value is +1 for depolarizing channels types (channels for which the equilibrium or reversal potential is less negative or more positive than the value θ, where θ is defined, as hereinabove, as the voltage at which the discrepancy is zero; in a spiking neuron, θ might be defined as the membrane voltage at spike threshold, or slightly more negative than spike threshold), and −1 for hyperpolarizing channel types (channels for which the reversal potential is less positive or more negative than θ). The anti-Hebbian-type algorithm of equation 3 then becomes w _(t+1) =w _(t) −αz U _(t)(V _(t)−θ)−βw _(t)  (6) and the Hebbian-type algorithm of equation 4 becomes w _(t+1) =w _(t) +αzR _(t) U _(t)(V _(t)−θ)−μw _(t)  (7) where the meanings of all characters other than ‘z’ are the same as in equations 3 and 4 hereinabove.

The invention describes how an “artificial neuron” could select its inputs. This neuron is described as a single compartment, meaning that the membrane voltage is always the same throughout the neuron, as would be the case if the neuron had no spatial extent. However, real neurons are extended in space, and thus membrane voltage is generally not the same throughout the neuron. A more realistic model of a neuron thus includes multiple compartments. Extension of the ideas presented herein to a multi-compartment neuron is contemplated. One way to do this would be to use the single compartment model described herein as a single compartment in a multi-compartment model. In such a case, the output or voltage of the neuron of the preferred embodiment would be replaced by the voltage of the one compartment within the multi-compartment neuron. The ‘inputs’ and ‘outputs’ would then apply just to the one compartment. If other compartments within the same neuron were to also follow the principles set forth herein, then they would have their own inputs and outputs. As recognized within the prior art, Hebbian and anti-Hebbian plasticity rules always rely exclusively on local information. Thus it is not difficult to extend the principles described herein from a single compartment to a multi-compartment neuron.

The single compartment of the artificial neuron of the preferred embodiment is presumed to correspond to the somatodendritic compartment of a neuron. However, in addition to having multiple dendritic compartments, real neurons also have synaptic terminals. There are numerous mechanistic differences between synapses and somatodendritic compartments. For example, the output of a somatodendritic compartment in a typical neuron corresponds to an action potential, whereas the output of a synaptic terminal corresponds to release (exocytosis) of a vesicle containing neurotransmitter molecules.

However, as discussed elsewhere (Fiorillo, 2008), a synaptic terminal may perform essentially the same information processing function as a somatodendritic compartment. In this analogy, the weighted sum of the activities of class 1 inputs would be replaced by the depolarization that accompanies arrival of an action potential, or by the subsequent rise in calcium concentration. Inputs of class 2, as well as class 3 and 4 in some embodiments, would contribute prior information that functions to predict and modify (either counteract or amplify) membrane voltage or calcium concentrations. A rise in calcium concentration triggers release of a vesicle. Thus calcium concentration is analogous to membrane voltage in the soma, and release of a vesicle is analogous to an action potential. High calcium concentration, or vesicle release, would correspond to a positive prediction error, or to a predictive amplification of the action potential input, depending on whether prior information sources (ion channels and other factors affecting free calcium concentration) were selected according to anti-Hebbian or Hebbian principles. The present invention should be broadly understood as specifying rules for selecting inputs to an ‘information processing element.’ In a neural network model, the element could correspond to any of multiple somatodendritic compartments, or to a presynaptic terminal.

It is important to recognize that references herein to “prediction” do not require any specific method or process of prediction. Predictions are always conditional on information, and information, by definition, predicts something. Thus the state of an ion channel (or the ‘activity’ of an input), or a set of ion channels, provides information and makes a prediction. The prediction can be quantified by a probability distribution, as described previously (Fiorillo, 2008). The plasticity rules modify the types of ion channel or inputs the neuron receives (by changing their weights), and thereby modify the predictions so as to improve their accuracy.

As will be understood by those familiar with the art, the invention may be embodied in other specific forms without departing from the spirit or essential characteristics thereof. Likewise, the particular naming and division of the members, features, attributes, and other aspects are not mandatory or significant, and the mechanisms that implement the invention or its features may have different names, divisions and/or formats. Accordingly, the disclosure of the invention is intended to be illustrative, but not limiting, of the scope of the invention, which is set forth in the following Claims. 

The invention claimed is:
 1. A computer-implemented method for processing information using an information processing element, said information processing element for receiving at least two classes of inputs and for computing an output, the method comprising the steps of: receiving, by said information processing element, a first class of inputs, each input having a weight value and an activity, said activity having information about a value of an external variable; receiving, by said information processing element, a second class of inputs, each input having a weight value and an activity, said activity corresponding to a weighted sum of past outputs of said information processing element, said second class of inputs further comprising two subclasses, a Hebbian subclass and an anti-Hebbian subclass, distinguished from one another by the type of plasticity rule regulating said weight values, said Hebbian subclass comprising a plurality of inputs, each of said inputs having a distinct activity, said activity corresponding to a weighted sum of past outputs of said information processing element: computing, by said information processing element, said output of said information processing element using a function of a weighted sum of said activities of said first class of inputs and said second class of inputs, using said weight values of said first class of inputs and said second class of inputs; and modifying said weight values of said inputs in said second class to predict said output, through use any of a Hebbian-type plasticity rule for inputs of said Hebbian subclass and an anti-Hebbian-type plasticity rule for inputs of said anti-Hebbian subclass, said plasticity rules utilizing said activity of an input and a discrepancy between said output of said information processing element and an intermediate reference value of said output; wherein a weighted sum of said activities of said second class of inputs effectively learns to predict and amplify a weighted sum of said first class of inputs, and said output therefore corresponds to a predictive amplification of said weighted sum of said first class of inputs.
 2. The computer-implemented method of claim 1, wherein said Hebbian-type plasticity rule incorporates information about a rewarding goal, and said output therefore becomes predictive of future reward.
 3. The computer-implemented method of claim 1, wherein weight values for said first class of inputs are modified through a Hebbian-type plasticity rule to maximize said discrepancy, and said external variable is thereby selected for its ability to generate variability in said output and to provide new information to said information processing element.
 4. The computer-implemented method of claim 3, wherein said Hebbian-type plasticity rule incorporates information about a rewarding goal, and said output therefore becomes predictive of future reward.
 5. The computer-implemented method of claim 1, further comprising the steps of: receiving, by said information processing element, a third class of inputs, each input having a weight and an activity, said activity having information about a value of an external variable; and computing, by said information processing element, said output of said information processing element using a function of a weighted sum of said activities of said first class of inputs and said second class of inputs and said third class of inputs, using said weight values of said first class of inputs and said second class of inputs and said third class of inputs; and modifying said weight values for said third class of inputs through an anti-Hebbian-type plasticity rule.
 6. The computer-implemented method of claim 1, wherein all said weight values of said Hebbian subclass have a constant value of zero, and said anti-Hebbian subclass is comprised of a plurality of inputs, each input having a weight value and an activity, said activity corresponding to a distinct weighted sum of past outputs of said information processing element, and said anti-Hebbian plasticity rule thereby acts on said anti-Hebbian subclass to enable said information processing element to learn to predict and counteract a weighted sum of said first class of inputs, and said information processing element thereby generates a prediction error as said output.
 7. The computer-implemented method of claim 1, wherein said method corresponds to an iterative process, said weights being modified repeatedly until some predetermined criteria is reached, thereby improving accuracy of prediction and causing said output of said information processing element to generate a temporal pattern that is dependent on the temporal pattern of a weighted sum of said activities of said first class of inputs.
 8. An apparatus for processing information using an information processing element, said information processing element for receiving at least two classes of inputs and for computing an output, the apparatus comprising: means for receiving, by said information processing element, a first class of inputs, each input having a weight value and an activity, said activity having information about a value of an external variable; means for receiving, by said information processing element, a second class of inputs, each input having a weight value and an activity, said activity corresponding to a weighted sum of past outputs of said information processing element, said second class of inputs further comprising two subclasses, a Hebbian subclass and an anti-Hebbian subclass, distinguished from one another by the type of plasticity rule regulating said weight values, said Hebbian subclass comprising a plurality of inputs, each of said inputs having a distinct activity, said activity corresponding to a weighted sum of past outputs of said information processing element; means for generating, by said information processing element, said output of said information processing element using a function of a weighted sum of said activities of said first class of inputs and said second class of inputs, using said weight values of said first class of inputs and said second class of inputs; and means for modifying said weight values of said inputs in said second class to predict said output, through use of a Hebbian-type plasticity rule for inputs of said Hebbian subclass and an anti-Hebbian-type plasticity rule for inputs of said anti-Hebbian subclass, said plasticity rules utilizing said activity of an input and a discrepancy between said output of said information processing element and an intermediate reference value of said output; wherein a weighted sum of said activities of said second class of inputs effectively learns to predict and amplify a weighted sum of said first class of inputs, and said output therefore corresponds to a predictive amplification of said weighted sum of said first class of inputs.
 9. The apparatus of claim 8, wherein said Hebbian-type plasticity rule incorporates information about a rewarding goal, and said output therefore becomes predictive of future reward.
 10. The apparatus of claim 8, wherein weight values for said first class of inputs are modified through a Hebbian-type plasticity rule to maximize said discrepancy, and said external variable is thereby selected for its ability to generate variability in said output and to provide new information to said information processing element.
 11. The apparatus of claim 10, wherein said Hebbian-type plasticity rule incorporates information about a rewarding goal, and said output therefore becomes predictive of future reward.
 12. The apparatus of claim 8, further comprising: means for receiving, by said information processing element, a third class of inputs, each input having a weight and an activity, said activity having information about a value of an external variable; means for computing, by said information processing element, said output of said information processing element using a function of a weighted sum of said activities of said first class of inputs and said second class of inputs and said third class of inputs, using said weight values of said first class of inputs and said second class of inputs and said third class of inputs; and means for modifying said weight values for said third class of inputs through an anti-Hebbian-type plasticity rule.
 13. The apparatus of claim 8, wherein all said weight values of said Hebbian subclass have a constant value of zero, and said anti-Hebbian subclass is comprised of a plurality of inputs, each input having a weight value and an activity, said activity corresponding to a distinct weighted sum of past outputs of said information processing element, and said anti-Hebbian plasticity rule thereby acts on said anti-Hebbian subclass to enable said information processing element to learn to predict and counteract a weighted sum of said first class of inputs, and said information processing element thereby generates a prediction error as said output.
 14. The apparatus of claim 8, wherein said apparatus is configured for iteratively processing, including means for said weights being modified repeatedly until some predetermined criteria is reached, thereby improving accuracy of prediction and causing said output of said information processing element to generate a temporal pattern that is dependent on the temporal pattern of a weighted sum of said activities of said first class of inputs.
 15. A non-transitory computer-readable storage medium storing one or more sequences of instructions for processing information using an information processing element, said information processing element for receiving at least two classes of inputs and for computing an output, which instructions, when executed by one or more processors, cause the one or more processors to carry out the steps of: receiving, by said information processing element, a first class of inputs, each input having a weight value and an activity, said activity having information about a value of an external variable; receiving, by said information processing element, a second class of inputs, each input having a weight value and an activity, said activity corresponding to a weighted sum of past outputs of said information processing element, said second class of inputs further comprising two subclasses, a Hebbian subclass and an anti-Hebbian subclass, distinguished from one another by the type of plasticity rule regulating said weight values, said Hebbian subclass comprising a plurality of inputs, each of said inputs having a distinct activity, said activity corresponding to a weighted sum of past outputs of said information processing element; computing, by said information processing element, said output of said information processing element using a function of a weighted sum of said activities of said first class of inputs and said second class of inputs, using said weight values of said first class of inputs and said second class of inputs; and modifying said weight value of one or more inputs in said second class to predict said output, through use of a Hebbian-type plasticity rule for inputs of said Hebbian subclass and an anti-Hebbian-type plasticity rule for inputs of said anti-Hebbian subclass, said plasticity rules utilizing said activity of an input and a discrepancy between said output of said information processing element and an intermediate reference value of said output; wherein a weighted sum of said activities of said second class of inputs effectively learns to predict and amplify a weighted sum of said first class of inputs, and said output therefore corresponds to a predictive amplification of said weighted sum of said first class of inputs.
 16. The computer-readable storage medium of claim 15, wherein said Hebbian-type plasticity rule incorporates information about a rewarding goal, and said output therefore becomes predictive of future reward.
 17. The computer-readable storage medium of claim 15, wherein weight values for said first class of inputs are modified through a Hebbian-type plasticity rule to maximize said discrepancy, and said external variable is thereby selected for its ability to generate variability in said output and to provide new information to said information processing element.
 18. The computer-readable storage medium of claim 17, wherein said Hebbian-type plasticity rule incorporates information about a rewarding goal, and said output therefore becomes predictive of future reward.
 19. The computer-readable storage medium of claim 15, further causing the one or more processors to carry out the steps of: receiving, by said information processing element, a third class of inputs, each input having a weight and an activity, said activity having information about a value of an external variable; computing, by said information processing element, said output of said information processing element using a function of a weighted sum of said activities of said first class of inputs and said second class of inputs and said third class of inputs, using said weight values of said first class of inputs and said second class of inputs and said third class of inputs; and modifying said weight values for said third class of inputs through an anti-Hebbian-type plasticity rule.
 20. The computer-readable storage medium of claim 15, wherein all said weight values of said Hebbian subclass have a constant value of zero, and said anti-Hebbian subclass is comprised of a plurality of inputs, each input having a weight value and an activity, said activity corresponding to a distinct weighted sum of past outputs of said information processing element, and said anti-Hebbian plasticity rule thereby acts on said anti-Hebbian subclass to enable said information processing element to learn to predict and counteract a weighted sum of said first class of inputs, and said information processing element thereby generates a prediction error as said output.
 21. The computer-readable storage medium of claim 15, wherein said steps of said one or more processors correspond to an iterative process, said weights being modified repeatedly until some predetermined criteria is reached, thereby improving accuracy of prediction and causing said output of said information processing element to generate a temporal pattern that is dependent on the temporal pattern of a weighted sum of said activities of said first class of inputs. 